EphemereUa (Cincticostella): A Revision of the Nymphal Stages

EphemereUa (Cincticostella): A Revision of the Nymphal Stages ( Ephemeroptera: Ephemerellidae) RICHARD K. ALLEN Reprinted Jrom Ta:z PAN~PA.cutc ENTOMOLOGIST Vol. 51, January, 1975, No. l PP 16-22 Made in United. States of America

16 THE PAN-PACIFIC ENTOMOLOGIST.E phemerella ( Cincticostella) : A Revision of the Nymphal Stages (Ephemeroptera: Ephemerellidae) RICHARD K. ALLEN 1 Department of Biology, California State University 5151 State University Drive, Los Angeles, California 90032 The following treatment includes a characterization of the subgenus Cincticostella, a description, or diagnosis, of the nymphal stages, a key to the nymphs, and the known distributional limits of each species. Ephemerella (Cincticostella) orientalis Tshernova, 1952, whose nymph is unknown is included with complete synonymy and known distribution. Grateful appreciation is expressed to Professors Kazimitzu Kato and Valentina Zaydman, California State University, Los Angeles, for translating parts of the papers by Imanishi (1940) and Tshernova (1972), respectively. SUBGENUS CINCTICOSTELLA ALLE'N nigra group Imanishi 1938: 33. Cincticostella Allen 1971: 513; Tshernova 1972: 614 (= Asiatella). Asiatella Tshernova 1972: 611. lmanishi (1938) placed E. nigra Ueno, 1928, in the nigra-group of the genus Ephemerella and Allen ( 1971) erected the subgenus Cincticostella for E. nigra and five other species. He transferred E. levanidovae Tshernova, 1952, and described E. castanea, E. delicata, E. imanishii, and E. insolta. Tshernova (1972) described the genus Asiatella to include E. nigra, E. femorata Tshernova, 1972, E. orientalis, E. levanidovae, and E. tshernovae Bajkova, 1962, to this taxon. In the same paper, as a footnote, she synonymized Asiatella with Cincti costella and placed E. imanishii as a junior synonym of E. tshernovae. Cincticostella is confined to southeast and eastern Asia. Ephemerella boja n. sp., E. gosei n. sp., and E. insolta are known from Thailand; E. castanea from Korea; E. delicata from Japan and Manchuria; E. femorata from Vietnam; E. levanidovae and E. orientalis from Russia; E. nigra from Japan; and E. tshernovae from Japan, Korea, and Russia. The number of described species in the subgenus is ten. The species of Cincticostella are all known from the nymphal stage except E. orientalis which was described from male and female subl The research upon which this report is baaed was supported by National Sciencea Foundation Grant No. GB-35591. THE PAN-PACIFIC ENTOMOLOGIST 51: 16-22. JANUARY 1975

VoL. 51, No. 1, JANUARY 1975 17 imagoes. Ephemerella nigra is the only species known from the nymph and the male imago. Nymphal Stage.-Body flattened ventrally, convex dorsally. Head round to quadrangular; genae often truncate; maxillae without apical canines, with apical tuft of setae; maxillary palpi well developed, vestigial, or absent. Fore femora with band of transverse spines near middle; denticles on tarsal claws variable in number. Anterolateral corners of prothorax produced anteriorly; mesothorax ex panded laterally in anterior portion. Abdominal terga with paired dorsal submedian tubercles; abdominal segments 7-9 with or without well developed posterolateral projections; abdominal terga 3-7 with lamellate, imbricated gills. Caudal filaments shorter than body. On the basis of nymphal characters two groups of related species are recognized. Ephemerella insolta, E. boja, and E. femorata form the insolta-group. These species are characterized by possessing suboc: cipital head tubercles, and the second and third pairs of femora are enlarged with serrated margins and/ or protuberances. The nigra-group includes E. nigra, E. castanea, E. delicata, E. gosei, E. levanidovae, and E. tshernovae. These species are without head tubercles and the second and third pairs of femora are narrow, not enlarged, and the mafgins are entire. Ephemerella orientalis cannot be placed to species-group until the nymphal stage is discovered. The characters most useful for distinguishing the species of Cincticostella nymphs are as follows: ( 1) the number and degree of development of the paired dorsal abdominal tubercles; (2) the degree of expansion, the presence or absence of marginal serrations, and the presence or absence of spines and tubercles on the anterior surfaces of the middle and hind femora; ( 3) the degree of development of the posterolateral projections on abdominal segments 7-9; ( 4) the shape of the genae; ( 5) the color patterns on the head and body; and ( 6) the relative lengths of the body and caudal filaments... The following key will serve to distinguish the known nymphs of the species of Cincticostella. Illustrations are not included but reference is made to previously published figures which are enclosed in parentheses in the couplets. That is, (Allen 1971: fig. 11) in couplet 1 makes reference to "New Asian Ephemerella with notes (Ephemeroptera: Ephemerellidae). Canad. Ent. 103: 512-528." KEY To THE NYMPHS OF EPHEMERELLA ( C1NcT1cosTELLA) 1. Middle and hind femora expanded and margins serrate; head with suboccipital tubercles (Gose 1969: fig. 23; Tshernova 1972: fig. 5) -------------------------------------------------------------------------------------------------------- in.solta-group, 2 -Middle and hind femora narrow, and margins entire (Allen 1971: fig.

18 THE PAN-PACIFIC ENTOMOLOGIST 9); head without suhoccipital tubercles (Allen 1971: fig. 13) ----------- ---------------------------------------- - ---- -- --------------------------------------------- nigra-group, 4 2 (1). Abdominal terga with paired submedian tubercles on segments 1-10 (Allen 1971: fig. 18) ; fore femora with median band of tubercles (Allen 1971: fig. 12); head, body and legs with numerous pale spots (Allen 1971: fig. 14) ----- ---------------------------------------------------------- insolta -Abdominal terga with paired submedian tubercles on segments 2--10 (Goee 1969: fig. 23) or 4-9 (Tshemova 1972: fig. 5); fore femora without a median band of tubercles; head, body and legs without pale spots -------------------------------- --------------- ------------------------------------------- 3 3 (2). Head quadrangular; abdominal terga with paired submedian tubercles on segments 2-10 (Gose 1969: fig. 23); known distributional limits Thailand --------------- --------------------- ------------------ --- -------------------- ---- boja -Head round; abdominal terga with paired submedian tubercles on segments 4-9 (Tshemova 1972: fig. 5); known distributional limits Vietnam --------------- ---- ---------- ------------------- ---------- ---- ---------- f emorata 4 (1). Head with three pale maculae on frons (Gose 1969: fig. 43); maxillae without palpi (Gose 1969: fig. 44); known distributional limits Thailand --------------------------------------------------------------------------------- --- ---------------- sosei -Head without pale maculae on frons; maxillae with pal pi; known distributional limits Manchuria, Korea, Japan, and Russia -------------------- 5 5 ( 4). Head with truncate genae (Tshemova 1952: fig. 78); middle and hind femora with an anterior longitudinal ridge --------------------------- levanidovae -Head with round genae (Allen 1971: fig. 13) ; middle and hind femora without a longitudinal ridge ------------------------- ------------ - --- ------------- 6 6 ( 5 ). Abdominal terga with paired submedian tubercles on segments 2-9 (Allen 1971: figs. 16-17); caudal filaments more than 70% as long as body (Imanishi 1940: fig. 18) ------------- ------ ------------ - -------------------- 7 -Abdominal terga with paired suhmedian tubercles on segments 5-9; caudal filaments less than 50% as long as body (lmanishi 1940: fig. 17) ------------------------------------------------ --------- ------------------- tshernovae 7 (6). Abdominal terga with dark sublateral stripes along line of suhmedlan tubercles (lmanishi 1940: fig. 18) ; body short, less than 7 mm in length ---- ---- ------------------------------------------------------- delicata -Abdominal terga unicolorous, often with a pale median stripe, without sublateral dark stripes; body moderately long, more than 9 mm in, length --------------------------- - -- ------- --------------- ----------- ---- ------ --- -- -------- 8 8 (7). Abdominal tubercles on segments 2-4 distinct and sharp (Allen 1971: fig. 17); body reddish-brown; known distributional limits Korea ----------------------------------- ------- ----------------- --------------- ----- ---------------- castanea -Abdominal tubercles on segments 2-4 barely discernible (Allen 1971: fig. 16); body dark brown to black, often with pale median longitudinal stripe; known distributional limits Japan ---------- --- ---------- nigra I Ephemerella ( Cinetieostella) boja, new species Ephemerella TEA Gose 1969: 132. This species was described and figured, but not named, from nymphs collected in Thailand. EphemereUa boja is a distinctive species with a

VoL. 51, No. 1, JANUARY 1975 19 quadrangular head and well developed posterolateral projections on segments 7-9. Nymph.-Length: body 11.0-12.0 mm; caudal fliaments 7.0-8.0 mm. General color brown. Head quadrangular; maxillary palpi small, two segmented. Thoracic nota without tubercles or ridges; prothorax much wider than head; anterior surface of femora smooth, without protuberances; fore femora small, margins entire; middle and hind femora broadly expanded laterally, margins serrate; tarsal claws with 3--4 denticles. Abdominal segments 3-9 with well developed posterolateral projections; terga 2-10 with paired submedian tubercles; tubercles small on terga 2-3, well developed on 4-10; segments 7-9 with well developed posterolateral projections. Caudal filaments brown (rewritten from Gose, 1969). Holotype nymph.-the specimen from which figure 23 in Gose was illustrated (Nature and Life in Southeast Asia, vol. VI. 1969) from Chanta Buri, Thailand, 20. VI-61, no other data, is designated as the type of the species. The other nymphal paratopotype is designated as a paratype. EPHEMERELLA (CINCTICOSTELLA) CASTANEA Allen Ephemerella castanea Allen, 1971: 514. Nymph.-Length: body 10.0-11.0 mm; caudal filaments 7.0-8.0 mm. General color reddish-brown with dark brown markings. Head without occipital tubercles; maxillary palpi with moderately developed palpi. Thoracic nota without tubercles or ridges. Abdominal terga 2-9 with paired submedian tubercles; tubercles on segments 2-4 small and sharp, always discernible; tubercles on segments 5-9 moderately developed. Caudal filaments brown with dark brown annulations at apex of each segment. Distribution.-South Korea, Kwang Nung and Seoul. EPHEMERELLA (CINCTICOSTELLA) DELICATA Allen Ephemerella "nay" Imanishi 1940: 206; Tshernova 1952: 274. Ephemerella delicata Allen 1971: 517. Nymph.-Length: body 5.5-7.0 mm; caudal filaments 5.5-7.0 mm. General color light brown to reddish brown and dark brown. Abdominal terga with paired submedian tubercles on segments 2--9; tubercles small on segments 2-4 and 9, well developed on segments 5-8; abdominal terga with dark submedian longitudinal stripes along line of submedian tubercles, pale medially and laterally, and with brown lateral maculae on segments 2--8. Caudal filaments with light thick setae on every second segment (rewritten from Imanishi 1940). Distribution.-Kamo River, Kyoto, Yanashiro Prefecture, Japan, and Botankosho, Sekito-ga, Manchuria. Remarks.-The following discussion is rewritten from Imanishi (1940): "Japanese specimens have white line on thorax, but these are absent on Manchurian collections. Abdominal markings are distinct on specimens from Manchuria, and indistinct or barely discernible on the Japanese. This species is almost identical to E. nigra in form and color, and the only difference is the smaller size and emergence is

20 THE PAN-PACIFIC ENTOMOLOGIST slightly later than E. nigra in Japan. The adult is unknown (adult probably smaller than E. nigra) and nymph is not as common as E. nigra." EPHEMERELLA ( CINCTICOSTELLA) FEMORATA Tshernova Asiatella femorata Tshernova 1972: 611, 614 (= Cincticostella). Nymph.-Length: body 12.0 mm; caudal filaments 5.0 mm. General color light brown. Head with paired suboccipital tubercles; genae rounded; maxillary palpi reduced in size, two segmented. Thoracic nota without tubercles or ridges; prothorax broadly expanded laterally; anterior surface of fore femora without protuberances, dorsal margin with small protuberances; middle and hind femora broadly expanded laterally; middle femora with apical serrations; hind femora with apical and dorsal serrations; femora, tibiae and tarsi margined with setae; tarsal claws with 2 denticles. Abdominal terga with paired submedian tubercles on segments 4-9, tubercles increase in length on posterior segments; segments 7-8 with well developed posterolateral projections. Caudal filaments dark brown at base (rewritten from Tshernova 1972). Distribution.-Red River (Song Koi), Back Thai, North Vietnam. Ephemerella ( Cineticostella) gosei, new species Ephemerella TEB Gose 1969: 135. This species, along with E. boja, was described and figured, but not named, by Gose (1969) from nymphs collected in Thailand. Nymph.-Length: body 6.0-7.0 mm; caudal filaments 3.0-4.0 mm. General color dark brown. Head round; frons with pale markings mesad to compound eyes and pale marking over median ocellus; genae truncate; maxillary palpi absent. Thoracic no ta without tubercles or ridges; tarsal claws with 6 denticles. Abdominal terga 2-9 with paired submedian tubercles; tubercles small on terga 2-3, better developed on 4-9. Caudal filaments light brown (rewritten from Gose 1969). H olotype nymph.-the specimen from which figure 38 was illustrated (Nature and Life in Southeast Asia, vol. VI, Gose 1969) from Chanta Buri, Thailand, 20. Vl-61, no other data, is designated as the type of the species. EPHEMERELLA (CINCTICOSTELLA) INSOLTA Allen Ephemerella insolta Allen 1971: 516. Nymph.-Length: body 5.0-6.0 mm; caudal filaments 4.0-5.0 mm. General color light brown to brown with numerous small pale spots on head, body and legs. Head with paired suboccipital tubercles; genae rounded; maxillary palpi present, but reduced in size. Thoracic nota with ridges; femora expanded laterally and with spines and protuberances; tarsal claws with 5-8 denticles. Abdominal terga 1-10 with well developed paired submedian tubercles; segments 7-9 without posterolateral tubercles. Caudal filaments brown. Distribution.-The species is known only from the type series collected from Chiengmai, Thailand.

VoL. 51, No. 1, JANUARY 1975 21 EPHEMERELLA (CINCTICOSTELLA) LEVANIDOVAE Tshernova Ephemerella levanidovae Tshernova 1952: 274; Tshernova 1958: 76; Edmunds 1959: 545; Allen 1971: 516; Tshernova 1972: 612. Nymph.-Length: body 12.0 mm; caudal filaments 10.0 mm. General color brown. Head without occipital tubercles; genae truncate; maxillae with well de veloped palpi. Thoracic nota without tubercles or ridges; femora of middle and hind legs with longitudinal ridge on anterior surface; tarsal claws with 6 denticles. Abdominal terga 5-8 with well developed tubercles, tubercles small on other segments. Caudal filaments with spines on every segment (rewritten from Tshernova 1952). Distribution.-This species is known only from the type series collected from the Hor River in eastern Russia. EPHEMERELLA (C1NcT1cosTELLA) NIGRA Ueno Ephemerella nigra Ueno 1928: 44; Imanishi 1937: 325; Ueno 1950: 128 (male genitalia); Edmunds 1959: 546; Bajkova 1962: 204; Allen 1971: 513; Tshernova 1972: 611. Chitonophora (?) nigra Ueno 1931: 224. Nymph.-Length: body 9.5-11.5 mm; caudal filaments 7.0--8.0 mm. General color dark brown to black. Head without occipital tubercles; genae round; maxillary palpi well developed. Thoracic nota without tubercles or ridges. Ah dominal terga 2-9 with paired suhmedian tubercles; tubercles on segments 2-4 barely discernible; tubercles on segments 5-9 moderately developed. Caudal filaments brown. Distribution.-This species has been reported from several localities on the Island of Honshu, Japan. EPHEMERELLA (CINCTICOSTELLA) ORIENTALIS Tshernova Ephemerella orientalis Tshemova 1952: 279; Tshemova 1958: 75; Tshernova 1972: 612. This species was described from a male imago collected in the vicinity of the Amur River in eastern Russia and the nymphal stage has not been associated at this time. Tshernova (1972) placed E. orientalis in Cincticostella (as Asiatella) with the following statement, "The imago described by me as E. orientalis Tshern. (Tshernova, 1952: 279, table XIV, fig. 99) due to the structure of the genital appendages is very close to E. nigra Ueno and by all means belongs to the genus A skztella." Distribution.-The adult of this species was described from Sudhuhynshi Preserve, USSR and records of additional specimens have not been published. EPHEMERELLA (CINCTICOSTELLA) TSHERNOVAE Bajkova Ephemerella "nax" Imanishi 1940: 205; Tshernova 1952: 274. Ephemerella tshernovae Bajkova 1962: 203; Tshernova 1972: 612, 614 (= imanishii). Ephemerella imanishii Allen 1971: 517.

22 THE PAN-PACIFIC ENTOMOLOGIST Ephemerella tshernovae nymphs are easily distinguished from those of the other species in the nigra-group as they possess paired submedian tubercles only on segments 5-9. Nymph.-Length: body 10.0-11.0 mm; caudal filaments 4.0 mm. General color reddish brown to dark brown with purple to purple black markings. Abdominal terga with large paired submedian tubercles on segments 5-9; abdomen with posterolateral projections on sgements 4-9; poorly developed on 4--6, well developed on 7-9; abdominal terga with short heavy setae; abdominal segment 9 with concave lateral margins. Caudal filaments less than one-half body length; caudal filaments with heavy setae around each segment (rewritten from lmanishi 1940). Distribution.-This species is reported by Imanishi (1940) from Gifu Prefecture, Japan, and four localities in Korea. LITERATURE CITED ALLEN, R. K. 1971. New Asian Ephemerella with notes (Ephemeroptera: Ephemerellidae). Canad. Entomol., 103: 512-528, 46 figs. BAJKOVA, 0. J. 1962. New species in the genus Ephemerella Walsh (Ephemerop tera: Ephemerellidae) from mountain tributaries of the Amur basin. Izvest. Trkhookeansk. Naurch. Issled. Inst. Rybu. Khoz. i Okeonog., 48: 202-205, 6 figs. EDMUNDS, G. F., Ja. 1959. Subgeneric groups within the mayfly genus Ephemerella (Ephemeroptera: Ephemerellidae). Ann Entomol. Soc. Amer., 52: 543-547. GosE, K. 1969. Mayflies (Ephemeroptera) from Thailand. Nat. Life SW Asia, 6: 125-138, 53 figs. IMANISHI, K. 1937. Mayflies from Japanese torrents. VII. Notes on the genus Ephemerella. Annot. Zool. Japon, 16: 321-329. lmanishi, K. 1938. Mayfiles from Japanese torrents. IX. Life forms and life zones of mayfly nymphs. Annot. Zool. Japon, 17: 23-26. lmanishi, K. 1940. Ephemeroptera of Manchouchuo, Inner Mongolia and Chozen. Rep. Limnobiol. Surv., Kwantung and Manchouchuo, (1940), pp. 169-263. TSHERNovA, O. A. 1952. Mayflies from the River Amur and neighboring waters, and their part in the nutrition of Amur-fishes. Trudi Amur. ichtiol. eksped., 1945-1949, 3: 229-360, 141 figs. TsHERNOVA, O. A. 1958. The geographical distribution of Ephemeroptera and ' some peculiar features of the fauna of the Amur Basin. Rev. Entomol., 37: 64-84, 5 maps. TsHERNOVA, 0. A. 1972. Some new species of may-flies from Asia (Ephemerop tera, Heptageniidae, Ephemerellidae). Rev. Entomol., 51: 604--614, 7 figs. UENO, M. 1928. Some Japanese mayfly nymphs. Mem. Coll. Sci. Kyoto imp. Univ., 6: 19-63. UENO, M. 1950. Ephemeroptera, pp. 120-130. Jn: lconographia Insectorum Japonicorum, 2nd ed., Tokyo.